Abstract
This study makes use of a procedure designed to illustrate, without serial section analysis, the three-dimensional changes in the ciliary axoneme produced by microtubule sliding, and to confirm essential features of the sliding microtubule hypothesis of ciliary movement. Cilia, isolated from Tetrahymena pyriformis by the dibucaine procedure, are attached to polylysine substratum, and treated with Triton X-100. Critical point drying maintains three-dimensional structure without embedding. The detergent removes the membrane and many axonemes unroll, always in an organized fashion so that doublets follow one another in sequence, according to the enantiomorphic form of the cilium. The central pair of microtubules fall to the side as a unit. The parallel doublet microtubules retain relative longitudinal positions in part by interdoublet or nexin links. Spoke organization and tip patterns are preserved in the opened axonemes. We generalize the work of Warner and Satir (Warner, F. D., and P. Satir, 1976. J. Cell Biol. 63:35-63) to show that spoke group arrangements are maintained for all doublets in straight regions, while systematic displacements occur in bent regions. The conclusion that local contraction of microtubles is absent in the axoneme is strengthened, and direct graphic demonstrations of sliding at the ciliary tip are shown. A morphogenetic numbering scheme is presented which results in a quantitative fit of the tip images to the images predicated by the equation for doublet sliding, and which makes possible new comparisons of structural parameters between axonemes and with cilia of other organisms.
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- AFZELIUS B. Electron microscopy of the sperm tail; results obtained with a new fixative. J Biophys Biochem Cytol. 1959 Mar 25;5(2):269–278. doi: 10.1083/jcb.5.2.269. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chasey D. Further observations on the ultrastructure of cilia from Tetrahymena pyriformis. Exp Cell Res. 1972 Oct;74(2):471–479. doi: 10.1016/0014-4827(72)90403-x. [DOI] [PubMed] [Google Scholar]
- Chasey D. The three-dimensional arrangement of radial spokes in the flagella of Chlamydomonas reinhardii. Exp Cell Res. 1974 Mar 15;84(1):374–380. doi: 10.1016/0014-4827(74)90418-2. [DOI] [PubMed] [Google Scholar]
- GIBBONS I. R. A method for obtaining serial sections of known orientation from single spermatozoa. J Cell Biol. 1963 Mar;16:626–629. doi: 10.1083/jcb.16.3.626. [DOI] [PMC free article] [PubMed] [Google Scholar]
- GIBBONS I. R. The relationship between the fine structure and direction of beat in gill cilia of a lamellibranch mollusc. J Biophys Biochem Cytol. 1961 Oct;11:179–205. doi: 10.1083/jcb.11.1.179. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gibbons B. H., Gibbons I. R. Flagellar movement and adenosine triphosphatase activity in sea urchin sperm extracted with triton X-100. J Cell Biol. 1972 Jul;54(1):75–97. doi: 10.1083/jcb.54.1.75. [DOI] [PMC free article] [PubMed] [Google Scholar]
- LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
- Linck R. W. Comparative isolation of cilia and flagella from the lamellibranch mollusc, Aequipecten irradians. J Cell Sci. 1973 Mar;12(2):345–367. doi: 10.1242/jcs.12.2.345. [DOI] [PubMed] [Google Scholar]
- Mazia D., Schatten G., Sale W. Adhesion of cells to surfaces coated with polylysine. Applications to electron microscopy. J Cell Biol. 1975 Jul;66(1):198–200. doi: 10.1083/jcb.66.1.198. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Satir B., Sale W. S., Satir P. Membrane renewal after dibucaine deciliation of Tetrahymena. Freeze-fracture technique, cilia, membrane structure. Exp Cell Res. 1976 Jan;97:83–91. doi: 10.1016/0014-4827(76)90657-1. [DOI] [PubMed] [Google Scholar]
- Satir P. Studies on cilia. 3. Further studies on the cilium tip and a "sliding filament" model of ciliary motility. J Cell Biol. 1968 Oct;39(1):77–94. doi: 10.1083/jcb.39.1.77. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Summers K. E., Gibbons I. R. Adenosine triphosphate-induced sliding of tubules in trypsin-treated flagella of sea-urchin sperm. Proc Natl Acad Sci U S A. 1971 Dec;68(12):3092–3096. doi: 10.1073/pnas.68.12.3092. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Summers K. E., Gibbons I. R. Effects of trypsin digestion on flagellar structures and their relationship to motility. J Cell Biol. 1973 Sep;58(3):618–629. doi: 10.1083/jcb.58.3.618. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Warner F. D. New observations on flagellar fine structure. The relationship between matrix structure and the microtubule component of the axoneme. J Cell Biol. 1970 Oct;47(1):159–182. doi: 10.1083/jcb.47.1.159. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Warner F. D., Satir P. The structural basis of ciliary bend formation. Radial spoke positional changes accompanying microtubule sliding. J Cell Biol. 1974 Oct;63(1):35–63. doi: 10.1083/jcb.63.1.35. [DOI] [PMC free article] [PubMed] [Google Scholar]